Effects of drought, disturbance, and biotic neighborhood on experimental tree seedling performance

Abstract Forest biodiversity is likely maintained by a complex suite of interacting drivers that vary in importance across both space and time. Contributing factors include disturbance, interannual variation in abiotic variables, and biotic neighborhood effects. To probe ongoing uncertainties and potential interactions, we investigated tree seedling performance in a temperate mid‐Atlantic forest ecosystem. We planted seedlings of five native tree species in mapped study plots, half of which were subjected to disturbance, and then monitored seedling survival, height growth, and foliar condition. The final year of data collection encompassed a drought, enabling comparison between intervals varying in water availability. Seedling performance was analyzed as a function of canopy cover and biotic neighborhood (conspecific and heterospecific abundance), including interactions, with separate generalized linear mixed models fit for each interval. All species exhibited: (a) pronounced declines in height growth during the drought year, (b) detrimental effects of adult conspecifics, and (c) beneficial effects of canopy openness. However, despite these consistencies, there was considerable variation across species in terms of the relevant predictors for each response variable in each interval. Our results suggest that drought may strengthen or reveal conspecific inhibition in some instances while weakening it or obscuring it in others, and that some forms of conspecific inhibition may manifest only under particular canopy conditions (although given the inconsistency of our findings, we are not convinced that conspecific inhibition is critical for diversity maintenance in our study system). Overall, our work reveals a complex forest ecosystem that appears simultaneously and interactively governed by biotic neighborhood structure (e.g., conspecific and/or heterospecific abundance), local habitat conditions (e.g., canopy cover), and interannual variability (e.g., drought).

. Drivers of seedling survival in species-specific models. Parameter estimates and SEs are displayed. CA(a), CA(c) = conspecific abundance (alive or cut); CO = canopy openness. Significance is indicated by symbology: grey border/line = p>0.05; black border/line = p<0.05; black fill = p<0.01.   Table S1. Conspecific abundance within local neighborhoods (10-meter radius) of planted seedlings. Values are medians, with 10 th and 90 th quantiles provided in parentheses. Because local neighborhoods necessarily overlap, values were first averaged within each plot, and then medians and quantiles were calculated at the plot level. Neighborhood abundance calculations were only done for seedling stations at which each focal species was planted, as these are the neighborhoods subject to conspecific effects analysis. For instance, because Cornus florida was not planted at the "Planted pine overstory" site (due to generally low abundance of this species at that site), there were no conspecific neighborhoods to evaluate, hence the "NA"

Generalized linear mixed models results, organized by species
Given the very high survival rates through the first summer (> 0.94 for all species), survival models were fit only for the two full-year intervals. In addition, foliar damage was not measured in 2020, so models for this response variable are provided only for August 2018 and 2019. Height growth models were fit for all three intervals.
Flowering dogwood (Cornus florida) survival was negatively associated with living conspecific abundance in the drought year, but not in the pre-drought year, and was unrelated to all other predictor variables (Fig. S2). C. florida height growth was linked to several predictors, but with no consistency across measurement intervals (Fig. S3). In the first summer, height growth was strongly positively associated with canopy openness and negatively associated with initial height. In addition, height growth was slighter greater in areas with higher living conspecific abundance. However, in the predrought year, this conspecific effect reversed, becoming strongly negative. In this same interval, heterospecific abundance also had a negative effect on height growth. No model predictors were significantly associated with height growth during the interval that spanned the drought. C. florida foliar damage in the first summer was greater for seedlings that were initially taller, in more exposed locations (higher canopy openness), and in areas with greater living conspecific abundance (Fig. S4). In 2019, foliar damage had no apparent relationship with any model predictors.
Sweetgum (Liquidambar styraciflua) survival in the pre-drought year was positively associated with canopy openness and negatively associated with living conspecific abundance (Fig. S2). In the year encompassing the drought, no model predictors were linked to L. styraciflua survival. L. styraciflua height growth was higher in areas with greater canopy openness, and this pattern held across all three measurement intervals (Fig. S3). Height growth was negatively linked to initial height in the first summer, but this predictor had no effect in subsequent intervals. In the drought year, heterospecific abundance had a negative influence on height growth, but no other intervals revealed a heterospecific effect. In the pre-drought year, there was a significant interaction between canopy openness and cut conspecific abundance. Cut conspecific abundance was positively linked to height growth in open canopy conditions, but negatively linked to height growth in less open conditions. L. styraciflua foliar damage was greater in the first summer on seedlings that were initially taller, and greater in 2019 on seedlings in locations with more canopy openness and higher living conspecific abundance (Fig. S4).
Tupelo (Nyssa sylvatica) survival was higher in areas with greater canopy openness in the droughtaffected year, but not in the pre-drought year, and was unrelated to any other predictor variables (Fig.  S2). N. sylvatica height growth was linked to several model predictors, two of which exhibited significant interactions (Fig. S3). Canopy openness was strongly associated with height growth in the first summer and pre-drought year, but not in the drought year. Initial height was negatively linked to height growth in the pre-drought and drought intervals, but not in the first summer. Locations with greater heterospecific abundance had lower height growth in the first summer, but this predictor had no apparent effect in later intervals. Canopy openness interacted with cut conspecific abundance in the first summer and pre-drought year, but the direction of the interaction differed across these two intervals. During the summer of 2018, increasing cut conspecific abundance led to decreased growth rates in darker areas, but from 2018 to 2019, increasing cut conspecific abundance led to increased growth rates in darker areas. In both cases, cut conspecific abundance was predicted to have little or no effect in more open areas. However, because the range of cut conspecific abundance in darker areas is limited, we are not comfortable reading much into these results. N. sylvatica foliar damage was also associated with several model predictors and an interaction (Fig. S4). In the first summer, higher living conspecific abundance was associated with greater foliar damage. In the pre-drought year, more foliar damage was observed on seedlings that were initially taller and planted in areas with greater canopy openness. Living conspecific abundance had no effect as a solo predictor in the pre-drought year, but there was a significant interaction with canopy openness: foliar damage was predicted to increase with living conspecific abundance, but only in open areas.
Black cherry (Prunus serotina) survival was unaffected by all model predictors in the pre-drought year, but -in the drought year -P. serotina survival was lower in areas with greater living conspecific abundance and higher in areas with greater heterospecific abundance (Fig. S2). P. serotina height growth was positively linked to canopy openness in the pre-drought and drought year (Fig. S3). Initial height was also predictive of height growth, but in an inconsistent manner; initially taller seedlings grew slower the first summer, but faster over the course of the following year. No other predictors were related to height growth. P. serotina foliar damage was greater in areas with more canopy openness, both in the first summer and the pre-drought year (Fig. S4). Foliar damage was lower in areas with higher heterospecific abundance, but only in the first summer.
Red maple (Acer rubrum) survival was apparently unaffected by the variables we included in our model (Fig. S2). No predictors were significant during the drought year, and the pre-drought survival model would not converge, mostly likely because of the high survival rate through that interval (0.93) and/or the low sample size relative to other species (only 72 seedlings planted). In the pre-drought year, A. rubrum height growth was greater in areas with more canopy openness, but this pattern did not manifest for the other intervals, and no other model predictors were significant (Fig. S3). A. rubrum foliar damage was greater in areas with higher living conspecific abundance, but in 2019 only (Fig. S4). Foliar damage was unrelated to all other variables. As with survival, the low A. rubrum sample size may have obscured some height growth and foliar damage relationships.

Supplemental discussion of Cornus florida findings
Looking comprehensively at our C. florida results, we see potential signals of complex dynamics linking numerous response and predictor variables, and spanning all analysis intervals. In the first summer (2018), C. florida seedlings exhibited greater foliar damage in more open locations and in areas with greater abundance of adult C. florida trees. However, in the same interval, C. florida seedlings grew faster in areas with greater canopy openness and higher conspecific abundance. Thus, two conditions that were positively associated with height growth (open canopy, proximate C. florida trees) were also associated with greater foliar damage. It is possible that positive plant-soil feedback helped with the early establishment of transplanted seedlings near adult conspecifics (Kardol et al. 2013), but that seedlings in these same locations experienced increased exposure to species-specific foliar pests and/or pathogens. Some of these agents may also benefit from a reduction in canopy cover, or perhaps inflict greater damage on faster growing seedlings (Züst and Agrawal 2017;Martini et al. 2021). No negative effects on growth or survival manifested that first summer, but height measurements the following year (2019) revealed that seedling growth was lower in areas with higher living conspecific abundance. As such, the foliar damage documented during the first summer may have led to reduced growth from 2018 to 2019. Furthermore, while nothing was predictive of C. florida survival from 2018 to 2019, living conspecific abundance was the sole significant predictor of survival from 2019 to 2020, and the association was negative. So, putting it all together, and aligning with previous studies that have detected conspecific inhibition in C. florida (Johnson et al. 2012;Bennett et al. 2017), one potential explanation is that young C. florida seedlings near conspecific adults are prone to foliar damage, which leads to reduced growth over the following year, and then to reduced survival rates the year after that. It is also possible that the stressful drought conditions of late summer 2019 acted in concert with lagging conspecific effects, and that the increased mortality by 2020 would not have occurred without the drought (Castagneyrol et al. 2018;Szczepaniec and Finke 2019;).
Digging deeper into the C. florida results, we can once again attempt to make sense of complex multi-year patterns, this time focusing on the ways in which drought may modify biotic neighborhood effects. Seedling height growth was negatively affected by living conspecific and heterospecific abundance prior to the drought, but both predictors became non-significant during the droughtimpacted interval. This could be because the drought stress overwhelmed other inhibitive effects orsimilarly -it could be that the lower growth rates simply made it more difficult to detect local neighborhood effects. We see a different pattern, however, for C. florida survival, with living conspecifics having no effect pre-drought, but then a negative effect on survival during the drought. This potential drought-mediated strengthening of conspecific inhibition is surprising given that several other studies have found drought-associated weakening (e.g., Newbery and Stoll 2013;Bachelot et al. 2015;Uriarte et al. 2018;Xi et al. 2022). However, it may be that the same negative conspecific mechanism (e.g., a species-specific foliar pathogen) manifests as slower growth in a non-drought year, but transitions into reduced survival in a more stressful, higher-mortality situation. Accordingly, it is possible that conspecific inhibition plays a temporally variable but important role in C. florida regeneration dynamics, perhaps helping to prevent the formation of a mono-dominant subcanopy layer.